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Vocal Stereotypy and Singing Behavior in Baiomyine Mice

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Vocal Stereotypy and Singing Behavior in Baiomyine Mice Journal of Mammalogy, 88(6):1447–1465, 2007 VOCAL STEREOTYPY AND SINGING BEHAVIOR IN BAIOMYINE MICE JACQUELINE R. MILLER* AND MARK D. ENGSTROM Department of Natural History, Royal Ontario Museum, 100 Queens Park, Toronto, Ontario M5S 2C6, Canada (JRM, MDE) Department of Ecology and Evolutionary Biology, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada (MDE, JRM) We examined spectral features that characterize the highly stereotyped, repetitive vocalizations of New World baiomyine rodents. Although stereotyped vocal signaling, described as ‘‘song,’’ has been documented in Scotinomys (singing or brown mice), its occurrence was unknown in the sister taxon Baiomys (pygmy mice). We also recorded vocalizations of females, about which little information was previously available. Although examination of morphological and molecular data supports a close relationship between the 2 baiomyine genera, we identified song as a complex behavior that further underpins the monophyly of the Baiomyini. Both spectral and temporal features render these songs highly localizable, a characteristic of possible utility for courtship and other social behavior. The song of Baiomys is confined entirely to the ultrasonic spectrum, unlike that of Scotinomys, which uses a broader range of frequencies. The intensity, identity, and predictability of vocalization suggest that these songs are purposeful and carry information important for species identification. Key words: Baiomyini, Baiomys, rodents, Scotinomys, song, stereotypy, ultrasound, vocal behavior ‘‘Nothing would work in the absence of communication.’’ within calls and songs (Catchpole and Slater 1995; Clark and (Hauser 1997) Wrangham 1993; Gil and Slater 2000; Hohmann and Fruth Animals communicate diverse information using vocal sig- 1994; Lengagne et al. 2001; Mitani et al. 1992; Mitani and nals, including identity, status, breeding condition, affective Marler 1989; Podos et al. 1992; Sloan et al. 2005; Zuberbu¨hler state, the likelihood of performing certain actions, and the char- 2002). These elements can be modified or reorganized to con- acteristics of environmental referents. These signals include vey a different message (e.g., Ackers and Slovodchidkoff 1999; loud ‘‘long calls’’ in mammals, which often encode information Win et al. 1981), or alter song attractiveness (see Catchpole and pertaining to territorial advertisement (e.g., Dempster et al. Slater [1995] for a review). 1992; Eisenberg and Lockhart 1972; Harrington 1983; The ability to locate conspecifics and maintain contact is Harrington and Mech 1979, 1983). Often stereotyped in either advantageous in territorial marking and reproductive behav- their form or in the manner of their repetition, these calls vary ior, as well as during social separation (Branchi et al. 2004; in complexity between taxa and in some species have been Hashimoto et al. 2001; Sales and Pye 1974). For animals that described as ‘‘song.’’ range broadly, or where maintaining social contact is difficult Songs are distinguished by how they are used, ‘‘being most when line of sight is lost, vocal signals can acquire charac- commonly given in the context of competition for resources teristics useful for both propagation and localization. Acous- (mates or food)’’ (Hauser 1997:95; see also Horn [1992] and tically, the ability to localize is facilitated by a number of Kroodsma [1982]). Songs also are distinguished from calls in mechanisms, such as when vocal signals are stereotypic (i.e., terms of structure and function, with songs tending to be longer signals that vary little in acoustic character or, if composed of in duration and more complex. In their entirety, they provide multiple elements, in chain structure), broadband or frequency taxonomic information and are useful tools to identify species modulated, repetitive, or ongoing (Lewis 1983; Sloan et al. and populations (Date et al. 1991; Geissman 1993; George 2005; Terhune 1974). The addition of temporal elements, such 1981; Haimoff et al. 1982; Thorpe 1961). A variety of studies as discrete terminal trailers, also can provide localizing cues also have identified distinct elements of meaning or syntax (Sloan et al. 2005). In alarm communication, the use of localizable calls can be advantageous if their emission allows the position of a threat to be monitored by distant conspecifics * Correspondent: [email protected] (Sloan et al. 2005). Yet localization increases the risk of predation for organisms that use such signals on a routine basis. Ó 2007 American Society of Mammalogists Moreover, high levels of stereotypy are likely expensive and www.mammalogy.org difficult to achieve for the sender (Eberhardt 1994; McCarty 1447 1448 JOURNAL OF MAMMALOGY Vol. 88, No. 6 Hafner 1978; Hooper and Carleton 1976; Packard 1960; Reid 1997; Sales and Pye 1974; this study). Some species are characterized by ecological or social conditions for which the ability to localize would be an asset (for instance, arboreal and monogamous mice). Few detailed acoustic analyses have been conducted on neotomines, or have they been presented in a phylogenetic context. This paper is part of an investigation of vocal behavior among the major lineages that constitute the Neotominae, with an emphasis on vocal stereotypy in taxa traditionally considered as peromyscines (Peromyscus and allied genera). The most spectacular of these signals are made by Scotinomys, a member of the tribe Baiomyini. Our focus is on vocal behavior in this tribe. The tribe Biaomyini includes 2 genera, Baiomys (pygmy mice) and Scotinomys (singing mice or brown mice), both comprised of 2 species (Musser and Carelton 2005). Scotin- omys is confined to premontane and montane moist forest in Central America, from Chiapas, Mexico, to western Panama. S. teguina occupies the northern and central parts of this range, whereas S. xerampelinus is restricted to Costa Rica and western Panama (Hooper 1972; Musser and Carleton 2005; Reid 1997). Areas of sympatry occur in Costa Rica, particularly the south- ern extent of the Central Cordillera such as Volca´n Irazu´, Volca´n Turrialba, and Volca´n Chiriqui, where the 2 species are segregated by altitude, ecology, and differences in vocal behavior (Hooper 1972; Hooper and Carleton 1976). The long calls of Scotinomys were described by Hooper and FIG.1.—Typical posture of male Scotinomys teguina associated Carleton (1976), including information for both S. teguina with stereotypic singing behavior. Both sexes of S. teguina and S. and S. xerampelinus, although a description of the vocaliza- xerampalinus exhibit similar posture during vocal displays. tions of females was presented for only S. teguina. The long call or ‘‘song’’ of Scotinomys is modulated temporally as well 1996; Zahavi 1980; see also Bradbury and Vehrencamp [1998] as in frequency and amplitude, and a sizeable fraction of the for a review). Thus, there is a trade-off among the social and songs’ energy is audible to the human ear. Individuals of both ecological benefits of producing localizable vocal signals, the species assume a characteristic posture while calling (Fig. 1): energetic costs associated with maintaining spectral character- reared up with neck extended and mouth agape (Hooper and istics that enhance propagation over distance, and the increased Carleton 1976; Reid 1997). The calls themselves are relatively risk of predation. This risk can be minimized when the fre- loud, and posturing contributes to acoustic resonant space quencies employed are above the hearing range of potential (Negus 1949). predators, typically meaning ultrasound. The 2 species of Baiomys occur at lower altitudes in drier, Ultrasound refers to frequencies above 15 kHz (Pye and more open habitats, including coastal prairie mixed scrub, post Langbauer 1998), although in the vernacular ultrasound tends to oak savanna, and mesquite–cactus from Texas to Mexico (B. refer to those frequencies above the upper threshold of human taylori—Eshelman and Cameron 1987), as well as arid weedy hearing (approximately 18–20 kHz; see for instance Hill and fields and dry brush throughout western and central Mexico Wyse 1989; see also Sales and Pye 1974:4). Vocal communi- (B. musculus—Packard and Montgomery 1978). There is only cation using ultrasonic frequencies has been routinely observed a small region of sympatry between the species of pygmy mice in a variety of muroid rodents (e.g., Galef and Jeimy 2003; Holy in west-central Mexico. In areas of overlap, the northern pygmy and Guo 2005; Lui et al. 2003; Moles and D’Amato 2000; Nyby mouse (B. taylori) occupies more grassy and xerophytic habi- and Whitney 1978; Okon, 1972; Sales and Pye 1974; tats than B. musculus, which ranges into zones with relatively Warburton et al. 1989). However, vocal signals within the higher humidity (Packard 1960). audible spectrum and with significant amplitude are rare in these Little is known about the vocal behavior of Baiomys. Blair taxa, possibly emphasizing their potential risk. Likewise, (1941:381) described the call of B. t. subater as a ‘‘high- although stereotypic vocalization, the use of ultrasound, and pitched, barely-audible squeal.’’ The call and posture assumed singing occur in a number of mammals, we know little about resembled the ‘‘singing’’ posture of Canis latrans, in that the these behaviors, their character, or function in mice. head appears ‘‘thrust forward and upward, stretching the The neotomine mice constitute a diverse assemblage of New throat’’ (Blair 1941:381), observations which were reiterated World
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